Review

Management of severe acute malnutrition in children

Steve Collins, Nicky Dent, Paul Binns, Paluku Bahwere, Kate Sadler, Alistair Hallam
Lancet 2006; 368: 19922000
Published Online
September 26, 2006
DOI:10.1016/S01406736(06)69443-9
Valid International Ltd, Oxford,
UK (S Collins MD, N Dent MSc,
P Binns RGN, P Bahwere MD,
K Sadler MSc, A Hallam BM BCh);
and Centre for International
Child Health, Institute of Child
Health, Guilford Street,
London, UK (S Collins, K Sadler)
Correspondence to:
Dr Steve Collins, Valid
International Ltd, Unit 14
Standingford House, 26 Cave
Street, Oxford
OX4 1BA
steve@validinternational.org

1992

Severe acute malnutrition (SAM) is dened as a weight-for-height measurement of 70% or less below the median, or
three SD or more below the mean National Centre for Health Statistics reference values, the presence of bilateral
pitting oedema of nutritional origin, or a mid-upper-arm circumference of less than 110 mm in children age 15 years.
13 million children under age 5 years have SAM, and the disorder is associated with 1 million to 2 million preventable
child deaths each year. Despite this global importance, child-survival programmes have ignored SAM, and WHO does
not recognise the term acute malnutrition. Inpatient treatment is resource intensive and requires many skilled and
motivated sta. Where SAM is common, the number of cases exceeds available inpatient capacity, which limits the
eect of treatment; case-fatality rates are 2030% and coverage is commonly under 10%. Programmes of
community-based therapeutic care substantially reduce case-fatality rates and increase coverage rates. These
programmes use new, ready-to-use, therapeutic foods and are designed to increase access to services, reduce
opportunity costs, encourage early presentation and compliance, and thereby increase coverage and recovery rates. In
community-based therapeutic care, all patients with SAM without complications are treated as outpatients. This
approach promises to be a successful and cost-eective treatment strategy.

Introduction
Severe acute malnutrition (SAM), is dened as a
weight-for-height measurement of 70% or more below
the median, or three SD or more below the mean National
Centre for Health Statistics reference values (that will
likely be replaced by new WHO growth curves1), which is
called wasted; the presence of bilateral pitting oedema
of nutritional origin, which is called oedematous
malnutrition;2 or a mid-upper-arm circumference of less
than 110 mm in children age 15 years.3,4 Many advanced
cases of SAM are complicated by concurrent infective
illness, particularly acute respiratory infection, diarrhoea,
and gram-negative septicaemia. By contrast, chronic
malnutrition (termed stunted) is dened by a
height-for-age indicator. In addition, a composite form of
malnutrition including elements of both stunting and
wasting is dened with a weight-for-age indicator. As
these dierent forms of malnutrition have dierent
causes and require substantially dierent treatments,
clear nomenclature to dierentiate them is needed.
Case-fatality rates in hospitals treating SAM in
developing countries average 2030% and have remained
unchanged since the 1950s5 despite the fact that clinical
management protocols capable of reducing case-fatality
rates to 15% have been in existence for 30 years. In 1992,
this failure to translate scientic knowledge of what is
needed to treat malnutrition into eective large-scale
interventions, was criticised as nutrition malpractice;6
13 years and numerous studies and clinical manuals
later, there is an even greater discrepancy between actual
practice in most institutions treating SAM and our
knowledge of what works.
The treatment of severe acute malnutrition occupies a
unique position between clinical medicine and public
health. The causes are essentially poverty, social exclusion,
poor public health, and loss of entitlement,7 and most cases
can be prevented by economic development and
public-health measures designed to increase dietary
quantity and quality alone, with no need for clinical input.

However, as acute malnutrition becomes more severe,

normal physiological mechanisms that adapt the organism
to low food intake become more pronounced.812 These
reductive adaptations aect every physiological function
in the body,1315 mobilising energy and nutrient reserves
and decreasing energy and nutrient demands; they are
initially benecial and allow the organism to maintain
homoeostasis. However, as the severity of nutritional insult
increases, these adaptations progressively limit the bodys
ability to respond to stresses such as infection.1517 In
practice, inpatient units treating SAM are commonly
confronted by extremely ill patients who need intensive
medical and nursing care. Most of these units are in the
poorest parts of the poorest countries and have severe
capacity constraints, in particular, very few skilled sta. In
addition, most carers of malnourished patients come from
the poorest families and have great demands on their time.
To achieve an impact at a population level, management
protocols must take these socioeconomic realities into
account, balancing the potentially conicting demands
and ethics of clinical medicine with those of public health.

Worldwide public-health signicance of

malnutrition
Malnutrition is a major public-health problem throughout
the developing world and is an underlying factor in over
50% of the 1011 million children under 5 years of age
who die each year of preventable causes.1821 However,
while the child-survival movement commonly acknowledges the importance of undernutrition, dened as low
weight for age,22 the importance of acute malnutrition is
seldom mentioned. For example, none of the ve papers
of the recent child survival series in The Lancet mention
acute malnutrition.22 This is a serious omission; acute
malnutrition is an extremely common disorder, associated
with high rates of mortality and morbidity and requiring
specialised treatment and prevention interventions.
Worldwide there are about 60 million children with
moderate acute and 13 million with severe acute
www.thelancet.com Vol 368 December 2, 2006

Review

malnutrition. About 9% of sub-Saharan African and 15%

of south Asian children have moderate acute
malnutrition23,24 and about 2% of children in developing
countries have SAM.24 In India alone, 28% of children
under 5 years of age (over 5 million children) are severely
wasted2527 and in many poor countries such as Malawi,
SAM is the commonest reason for paediatric hospital
admission.28
The risk of mortality in acute malnutrition is directly
related to severity: moderate wasting is associated with a
mortality rate of 30148 per 1000 children per year29,30 and
severe wasting is associated with a mortality rate of
73187 per 1000 children per year.29 This equates to over
15 million child deaths associated with severe wasting
and 35 million with moderate wasting every year. These
numbers do not include children who die of oedematous
malnutrition (kwashiorkor), a form of SAM that in some
countries is more common than the wasted form, and
probably, therefore, underestimate the total number of
child deaths directly associated with acute malnutrition
(table).

High case-fatality rates for SAM

Over the past 50 years, in most resource-poor settings,
case-fatality rates for severe malnutrition treated in health
facilities have remained at 2030% for marasmus
(wasting malnutrition) and up to 5060% for
kwashiorkor.5,31 By contrast, since the 1970s there have
been management protocols capable of achieving
case-fatality rates of 15%,15,32,33 and well-resourced
humanitarian agencies using these protocols frequently
achieve mortality rates under the 10% level stipulated in
the international Sphere Project standards.4,34,35

Current management protocols

At present, an exclusive inpatient approach to the clinical
care of SAM is recommended. The core of accepted
Regions

Wasting numbers
(1000)

Annual mortality numbers

Moderate Severe
and severe

2 Z scores
below WFH

23 Z scores
below WFH*

>3 Z scores
WFH

106 394

10

10 639

3192

565 768

421 767

987 535

44 478

3114

890

168 942

117 547

286 489

South Asia

166 566

15

24 985

3331

1 644 950

440 201

East Asia and Pacic

159 454

6378

484 528

Latin America and Caribbean

54 809

1096

83 273

CEE-CIS and Baltic states

30 020

1201

300

68 416

49 182

10 929

2 905 951

Sub-Saharan Africa
Middle East and north Africa

Industrialised countries
Developing countries

Under-5 population Wasting prevalence

2000 (1000)
(%)

WHO management protocols is ten steps in two phases

(stabilisation and rehabilitation).2,3639 The approach
requires many trained sta and substantial inpatient bed
capacity. Where these are available and sucient
attention is paid to the quality of care, there is good
evidence that these protocols can substantially decrease
case-fatality rates in both stable environments33,4044 and
during emergency humanitarian interventions.34,45
However, despite the success of these protocols when
implemented in specialised units, their publication has
not led to widespread decreases in case-fatality rates in
most hospitals in the developing countries.46,47
The persistence of high case-fatality rates is commonly
attributed to inappropriate case management as a result
of poor knowledge.5,48 The accepted view is that wider
implementation of the WHO guidelines through
in-service training and incorporation into medical and
nursing curricula is the key to substantially decreasing
case-fatality rates worldwide.25,37,4952 However, whereas
there is good evidence that adequate training of health
sta in the management of SAM is essential if the
implementation of the WHO guidelines is to be eective,
the evidence base supporting the view that the wider
implementation of the WHO guidelines is key to the
reduction of case-fatality rates is weak. There have been
no published controlled trials looking at the eect of the
use of the WHO protocol in operational settings. In their
absence, the evidence of the positive eects of these
protocols comes from observational studies done in a
few selected hospitals or well-resourced, nongovernmental-organisation, humanitarian operations.
These studies all suggest that the availability of sucient
resources,53 particularly skilled and motivated health
sta, is a vital determinant of success and eectiveness.
In practice, the many skilled sta needed are rarely
available. For example, in Malawi in 200304 there were
only 113 physicians and 256 nurses per 100 000 people,54

50 655

3 Z scores
below WFH

546 471

Least developed countries

110 458

10

Total

707 584

2 085 151

39 668
-

Total

484 528
83 273
108 084

1 444 214

4 350 164

11 046

2209

671 290

291 918

963 209

60 228

13 139

3 577 241

1 736 132

5 313 373

Population and prevalence of wasting from UNICEF global database on child malnutrition 2001.24 CEE-CIS=Central and Eastern Europe and Commonwealth of Independent
States. WFH=weight-for-height index. *Moderate mortality rate=76/1000/year (average of nine studies range 30148 for children with <80% weight for height or
2 Z scores).29 Severe mortality rate=132/1000/year (average of ve studies, range 73187 children with mid-upper-arm circumference <110 mm).29

Table: Worldwide burden of acute malnutrition in children aged less than 5 years

www.thelancet.com Vol 368 December 2, 2006

1993

Review

15 of the 26 districts had on average fewer than 15 nurses

per facility, and ve districts had fewer than one nurse
per facility; there were ten districts without a Ministry of
Health doctor, and four districts without any doctor
(Vujicic M, World Bank, personal communication).
Perhaps as a result of these constraints, the use of similar
protocols had little eect on CFRs in nutrition
rehabilitation units in Malawi, only reducing them from
25% to 20%.55 The paucity of skilled health sta is not
restricted to Malawi and in 20 of the African countries
most aected by acute malnutrition there are fewer than
four doctors and 22 nurses per 100 000 people.54 The
World Bank has identied the lack of skilled human
resources as a fundamental constraint to the
improvement of health outcomes and the reaching of
Millennium Development Goals.56 In practice, shortages
of skilled sta commonly preclude the eective and
sustainable implementation of WHO guidelines for the
management of SAM.

Eect of HIV and tuberculosis

HIV and tuberculosis are increasing the workloads of
hospital units treating SAM through both the direct
eects of infection and the indirect negative eects on
livelihoods and food security. HIV and tuberculosis
infection decrease skilled human resource capacity in
health services, raise the prevalence of SAM, and
increase case-fatality rates.43,44,57,58 In sub-Saharan Africa,
a high proportion of severely malnourished children
admitted to nutritional rehabilitation units are now also
HIV positive,55,5763 particularly those with marasmus.57,59
In 2000 in Malawi for example, 34% of the severely
malnourished children admitted to the Blantyre Queen
Elizabeth hospital nutritional rehabilitation unit were
HIV positive.57 Although experience in resource-poor,
sub-Saharan countries has shown that many
HIV-positive children can recover normal nutritional
status when given standard treatment protocols for
SAM without antiretroviral drugs,58,64 their recovery is
slower than that of uninfected children. HIV infection
is also associated with high rates of complication and
case fatality.55,57,59

Treatment at home and in the community

Concerns over the limited capacity of hospital units to
treat SAM are not new. Since the 1960s, the high cost and
poor success rates of inpatient treatment have prompted
debate over whether hospitals were the best places to
treat SAM.65,66 There are several well-known weaknesses
of a centre-based approach: limited inpatient capacity
and lack of enough skilled sta in hospitals to treat the
large numbers needing care;67,68 the centralised nature of
hospitals promotes late presentation and high opportunity
costs for carers; and the serious risks of cross infection
for immunosuppressed children with SAM and the high
mortality rates before and after discharge.31,6972 These
concerns persist today.73
1994

In the 1970s, these problems prompted moves to

demedicalise the treatment of SAM and move the locus
of treatment away from hospitals to communities, into
either simple nutrition rehabilitation centres, existing
primary health-care clinics, or the homes of those
aected.31,74 The results from early outpatient treatment
programmes were variable. Some achieved low mortality
and positive eects on growth while children were
attending nutrition rehabilitation centres, but usually
these benets were not maintained after discharge.7577 In
others, mortality and relapse rates both during treatment
and after discharge were high72,78 and rates of weight gain
were low.79,80 The requirement for children to attend each
day and eat in the nutrition rehabilitation centres has
also resulted in low programme coverage, often proving
to be unpopular with mothers and resulting in high
default rates.42
In 2001, Ashworth reviewed 27 such programmes from
the 1980s and 1990s.81 Only six (22%) of the 27 achieved
case-fatality rates of less than 5%, average weight gains of
more than 5 g/kg/day, and relapse or readmission rates
of less than 10%Ashworth concluded that home
treatment is rarely successful81 and that the early
discharge of severely malnourished patients from
inpatient treatment units is usually hazardous.52 In 2005,
Ashworth updated her review to include an additional six
studies of ready-to-use therapeutic food. Five (83%) of
these six studies were considered to be successful; a far
greater success rate than in those studies not using
ready-to-use therapeutic food.82
Two other programmes, both in Bangladesh, have
reported successful rehabilitation of children with SAM
discharged to home care after 1 week of inpatient
management with mixtures of local foods combined with
the provision of multivitamins and minerals.42,83 The costs
for home-based treatment of US$29 and US$2230 were
substantially lower than those of US$156 and US$7460
for hospital care.83,84 Similar improvements in
cost-eectiveness of care were seen in home-treatment
programmes in Jamaica.85

Ready-to-use therapeutic food

The Ashworth review indicates that the recent
development of ready-to-use therapeutic food has greatly
eased the diculties associated with providing a suitable
high-energy, nutrient-dense food that is safe for use in
outpatient programmes. Ready-to-use therapeutic food is
an energy-dense food enriched with minerals and
vitamins, with a similar nutrient prole but greater energy
and nutrient density than F100, the diet recommended by
WHO in the recovery phase of the treatment of SAM.86 In
contrast to the water-based F100, ready-to-use therapeutic
food is an oil-based paste with an extremely low water
activity.87 As a result, ready-to-use therapeutic food does
not grow bacteria even when accidentally contaminated,88
allowing it to be kept unrefrigerated in simple packaging
for several months. As the food is eaten uncooked,
www.thelancet.com Vol 368 December 2, 2006

Review

heat-labile vitamins are not destroyed during preparation

and the labour, fuel, and water demands on poor
households are minimised. The production process is
simple, and ready-to-use therapeutic food can be made
from local crops89 with basic technology that is readily
available in developing countries.90,91
In a clinical trial in severely malnourished children in
Senegal, energy intakes (808 kJ/kg/day vs 573 kJ/kg/day,
p<0001), rates of weight gain (156 g/kg/day vs
101 g/kg/day, p<0001) and time to recovery (173 days
vs 134 days, p<0001) were all signicantly greater in
those receiving ready-to-use therapeutic food than in
those receiving F100.92 Trials in Malawi have also
successfully used a take-home ration given to children in
the recovery phase of the treatment of SAM. In one, a
take home ration of 730 kJ/kg/day (175 kcal/kg/day)
successfully rehabilitated HIV-negative, severely
malnourished children, after early discharge from a
nutrition rehabilitation units providing initial, phase-one
care according to WHO protocols. Rates of weight gain
(52 g/kg/day vs 31 g/kg/day) and the proportion of
children recovering to 100% weight for height (95% vs
78%, relative risk [RR] 12, 95% CI 1113) were
signicantly better in the ready-to-use therapeutic food
groups when compared with groups receiving a larger
amount of energy from cornsoya-blend our supplied
by the World Food Programme.28 In the same trial, 56%
of the HIV-positive children treated with ready-to-use
therapeutic food also achieved 100% weight for height.64
In another trial implemented in rural nutritionrehabilitation units, 730 kJ/kg/day of locally made
ready-to-use therapeutic food given during the
rehabilitation phase of treatment produced signicantly
better rates of weight gain (35 g/kg/day vs 20 g/kg/day),
recovery (79% vs 46%, RR 28 95% CI 2531), and
mortality (30 vs 54%, OR 05, 95% CI 0307) than
did the standard inpatient treatment with F100, followed
by outpatient supplementation with a large one-o ration
(50 kg) of corn-soya-blend our.93 However, the rates of
weight gain on the ready-to-use therapeutic food regime
were far lower than the 1015 g/kg/day that can be
achieved with a ration of 730 kJ/kg/day. The combination
of low rates of weight gain and low mortality rates
indicates that this was probably due to sharing of the
ration.
The development of ready-to-use therapeutic food has
allowed much of the management of SAM to move out of
hospitals. By shortening the duration of inpatient
treatment from an average of 30 days to only 510 days,
the move towards using ready-to-use therapeutic food in
the recovery phase of treatment reduces the resources
needed to treat SAM, which improves cost-eectiveness.
The provision of phase-one inpatient care for all cases,
however, still requires substantial resources and entails
substantial opportunity costs for carers. A requirement for
inpatient care also means that programmes must be
implemented from hospitals and large clinics with
www.thelancet.com Vol 368 December 2, 2006

inpatient facilities. Centralised treatment increases

barriers to access for rural communities where acute
malnutrition is most prevalent. Increased barriers to
access and opportunity costs serve to delay presentation,
making the disorder harder to treat, and increase the
number of patients with complications. These barriers
increase costs and case-fatality ratios55 and decrease the
proportion of severely malnourished children who are
able to access treatment, thereby reducing coverage
(unpublished).

Community-based management of acute

malnutrition
During the past 5 years, a growing number of countries
and international relief agencies have adopted a
community-based model for the management of acute
malnutrition, called community-based therapeutic
care.9497 This model provides a framework for an
integrated public-health response to acute malnutrition,
treating most patients with SAM solely as outpatients and
reserving inpatient care for the few with SAM and
complications.73 The model also aims to integrate
treatment with various other interventions designed to
reduce the incidence of malnutrition and improve public
health and food security. Programme design attempts to
take into account the socioeconomic factors, particularly
poverty, high workloads for women, and the exclusion
from health and education services that contribute to the
late presentation of cases of acute malnutrition.
Programmes are therefore very decentralised to minimise
geographical barriers to access73 and include intensive
community consultation and mobilisation to maximise
understanding and participation. This design minimises
the costs to families and maximises access to treatment.98
The decentralised design also means that, in
non-emergency situations, there are few cases of SAM at
any one access point and the quantities of ready-to-use
therapeutic food required to treat them are therefore
small. In current Ministry of Health implemented
programmes in Malawi, for example, a health-centre
treating 15 children with SAM per month requires 160 kg
(eight boxes) of ready-to-use therapeutic food. This small
quantity can be delivered easily together with other
routine health supplies. This eases the problems
associated with integrating community-based therapeutic
care into existing health services, even in resource-poor
settings.
The use of mid-upper-arm circumference as the sole
anthropometric indicator for screening and admission
into community-based therapeutic care also facilitates
community participation, helping to devolve responsibility
for selection of patients towards the community.
Mid-upper-arm circumference is an indicator of acute
malnutrition that reects mortality risk99102 and has
recently been endorsed as an independent criterion for
admission into therapeutic feeding programmes by an
informal consultation of WHO.103,104 The use of this
1995

Review

measure requires no complicated equipment and can

easily be taught to community-based workers, making it
practical for use in resource-poor settings.105,106
Community-based therapeutic cares clinical approach
is based on the fact that the severity of SAM, its prognosis,
and the determinants of successful treatment are
primarily dependent on the time to presentation.28,30,55,68,99,107,108 SAM is classied on the basis of whether
there are coexistent life-threatening complications109
(gure). Children presenting with SAM complicated by
life-threatening illness receive inpatient care according
to the WHO treatment protocols. Those with SAM but
without life-threatening complications are treated
through weekly or fortnightly attendance in outpatient
therapeutic programmes. In outpatient therapeutic
programmes, they receive an 837 kJ/kg/day
(200 kcal/kg/day) take-home ration of ready-to-use
therapeutic food, a course of oral broad-spectrum
antibiotics, vitamin A, folic acid, anthelminthics and, if
appropriate, antimalarials. To increase access to treatment
and encourage earlier presentation, outpatient therapeutic
programmes are decentralised and implemented through
standard primary health-care units or even non-permanent
access points. This approach results in most children
presenting at a stage when they can still be treated
eectively as outpatients by front-line health sta, which
greatly reduces the need for trained clinic sta, thereby
easing integration into routine health services.
Case-fatality rates among 23 511 unselected severely
malnourished children treated in 21 programmes of
community-based therapeutic care in Malawi, Ethiopia,
and Sudan, between 2001 and 2005, were 41%, with
recovery rates of 794% and default rates of 110%. 74%
of these severely malnourished children were treated
solely as outpatients.94,95,103 Coverage rates for nine of these
programmes have been estimated with a new
coverage-survey technique designed to provide more
precise coverage estimates of health-care programmes.110
Average coverage was 725%,95,103 substantially higher
than coverage rates seen in comparable centre-based
programmes which are often less than 10%.111,112 Similar
positive results have recently been published from Niger,
where Mdecins Sans Frontires (MSF) cared for more
than 60 000 children with SAM with an approach based
on outpatient therapeutic programmes. About 70% of
patients were treated solely as outpatients and overall
case-fatality ratios were about 5%.113
Community-based therapeutic care has also shown
promise as an intervention to assist children with SAM
infected with HIV. A cohort trial in Malawi assessed the
eectiveness of community-based therapeutic care in the
treatment of SAM in HIV-positive and HIV-negative
children and examined its use as an entry point for
home-based care programmes targeting people living
with HIV/AIDS.114 59% of the severely malnourished
HIV-positive children not receiving antiretroviral drugs
recovered compared with 834% of the HIV-negative
1996

Severe acute
malnutrition

Without complications

With complications

1 Bilateral pitting
oedema grade 3*
(severe oedema)

MUAC <110 mm

or

Bilateral pitting oedema

grades 1 or 2* with
MUAC 110mm

or

2 MUAC <110mm
and bilateral pitting
oedema grades 1 or 2
(marasmic kwashiorkor)

and
Appetite
Clinically well
Alert

or
3 MUAC <110mm or
bilateral pitting oedema
grades 1 or 2
and one of the following:
Anorexia
Lower-respiratory-tract
infection
Severe palmar pallor
High fever
Severe dehydration
Not alert

Inpatient care
IMCI/WHO protocols

Outpatient therapeutic
care protocols

Figure: Classication of severe acute malnutrition used in community-based

therapeutic care
MUAC=mid-upper-arm circumference. ICMI=Integrated Management of
Childhood Illness. *Grade 1=mild oedema on both feet or ankles;
grade 2=moderate oedema on both feet, plus lower legs, hands, or lower arms;
grade 3=severe generalised oedema aecting both feet, legs, hands, arms, and
face. IMCI criteria:39 60 respirations/min children age <2 months;
50 respirations/min for age 212 months; 40 respirations/min for ages
15 years; 30 respirations for age >5years.

children (p<0002, unpublished). However, at a mean

follow-up of 15 months after discharge, 53% of
HIV-positive children had relapsed into moderate acute
malnutrition compared with 104% of the HIV-negative
children. HIV-positive children therefore need continual
community-based monitoring after discharge and, for
treatment to be optimally eective, community-based
programmes for SAM must be integrated with
home-based care and antiretroviral-drug programmes
for HIV. In this study, the uptake rate for voluntary
counselling and testing for children attending the
programme was greater than 90%, far greater than
usually seen in Malawi (unpublished). This nding
shows a high potential for synergy and integration
between community-based therapeutic care, home-based
care, and antiretroviral-drug programmes for HIV.
Programmes of treatment for SAM tend to be highly
cost eective in terms of additional years of life gained
www.thelancet.com Vol 368 December 2, 2006

Review

because they precisely target resources at children with a

very high mortality risk. Initial data indicate that the
cost-eectiveness of emergency community-based
therapeutic care is comparable to mainstream
child-survival interventions, such as vitamin-A provision
or oral rehydration therapy for diarrhoeal disease.
Estimates from two established emergency programmes
were US$101197 per admission which is equivalent to
between US$12 and US$132 for each year of life gained
dependent on the assumptions made for the mortality
rates of untreated SAM.115 The exact gure depends on the
density and prevalence of severe acute malnutrition, the
numbers of acutely malnourished children treated, the
infrastructure present, accessibility, and the estimation of
case-fatality ratios in untreated SAM.103,115 Although these
are broad ranges, they are below the $150 threshold
described by the World Bank as highly cost-eective. The
development of local production of ready-to-use
therapeutic food with new cheaper recipes based on locally
available grains and pulses should further reduce costs.

Conclusion
Where sucient resources are available, the WHO
inpatient treatment model for SAM can achieve low
case-fatality rates. However, exclusive inpatient
treatment strategies are resource-intensive and require
many skilled sta. Because the prevalence of SAM is
highest in resource-poor environments, there is usually
a substantial mismatch between the many patients
requiring treatment and few skilled sta and scarce
resources available to treat them. The HIV/AIDS
pandemic is further lowering resource availability and
increasing the numbers of acutely malnourished
children, aggravating this mismatch and increasing
case-fatality rates.
New approaches for the management of SAM, such as
community-based therapeutic care, complement the
existing WHO inpatient protocols. These programmes
use ready-to-use therapeutic food to treat most children
suering from SAM as outpatients, reserving inpatient
treatment for those with complications. They are
designed to decrease barriers to access, encourage earlier
presentation, reduce opportunity costs associated with
treatment, and encourage compliance by patients.
Treatment of most patients with SAM solely as outpatients
reduces inpatient caseloads to more manageable levels,
which helps decongest crowded inpatient units, decreases
the risks of nosocomial infection, and increases the time
available to sta to devote to the sickest children. These
new approaches have greatly reduced case-fatality rates
and increased coverage ratesinitial data indicate that
they are very cost eective.

The way forward

Community-based therapeutic care should now be scaled
up in both emergency and non-emergency settings and
appropriate training included in medical, nursing, and
www.thelancet.com Vol 368 December 2, 2006

primary health-care curricula. To start this process,

WHO, UNICEF, and the UN Standing Committee on
Nutrition recently convened an informal consultation on
the community-based management of severe
malnutrition in children. The meeting began the process
of incorporating these techniques into the WHO
guidelines.103 This is an essential step. However,
improvements in treatment protocols, programme
design, and training are, by themselves, insucient. If
community-based therapeutic care is to attain its
maximum potential in reducing avoidable child mortality,
there must be changes in funding priorities and child
survival strategies. Leveraging these changes will require
strong evidenced-based advocacy highlighting the global
importance of SAM and communicating clearly the fact
that highly cost-eective interventions exist.
WHO should adopt the term acute malnutrition to
dierentiate wasting and oedematous malnutrition from
growth faltering and stunting. Acute malnutrition has
dierent causes, dierent indicators, and requires
dierent interventions to chronic malnutrition. Without
a clear and appropriate nomenclature these dierences
are obscured, which results in confusion over treatment
strategies and mixed messages going out to
policymakers.
Second, the global importance of SAM as a major cause
of avoidable mortality must be better communicated and
the child survival agenda must give greater priority to
treatment of the disorder. This requires SAM to be
included as a specic cause of death in
mortality-surveillance data and included as a diagnosis in
standard morbidity surveillance. Without this, the high
numbers of deaths and high morbidity attributable to
SAM will continue to go unrecorded and un-noticed.
Third, nutritionists should communicate the fact that
there are successful and highly cost-eective interventions
for SAM. Although the hospital-based treatment of SAM
is more cost-eective than many of the mainstream
child-survival interventions, such as treatment of severe
diarrhoea in hospitals or vitamin-A distribution,112,116 this
has been poorly communicated to policymakers and
funders. Community-based therapeutic care promises to
increase this cost-eectiveness further. There is a need
for more cost eectiveness data and for these ndings to
be communicated to policymakers.
Last, an appropriate indicator of acute malnutrition, such
as mid-upper-arm circumference, should be included as a
standard element in both growth monitoring programmes
and integrated management of childhood illness to allow
these programmes to diagnose acute malnutrition more
eectively. This indicator is essential if cases of SAM are
to be caught early, before complications arise and while
cheap outpatient treatment is possible. At present,
growth-monitoring programmes do not include any
indicator of acute malnutrition and integrated management
of childhood illness includes only visible severe wasting,
an indicator that is subjective, dicult to use in practice,
1997

Review

and unreliable.104,117 Mid-upper-arm circumference is easy

to use and ecient at identifying those children who need
specialist interventionswithout this, most cases of SAM
will go undiagnosed and untreated.
Achieving the fourth Millennium Development Goal of
a two-third reduction in childhood mortality will not be
possible unless SAM is addressed eectively. For
interventions to full their potential, policymakers must
give SAM an urgency commensurate with its global
importance as a leading cause of preventable childhood
mortality.
Conict of interest statement
The authors work for Valid International Ltd, an organisation that has
been engaged in the research and development of community-based
therapeutic care. S Collins and A Hallam are also unpaid directors of
Valid Nutrition, a not-for-prot company established to research and
manufacture ready-to-use therapeutic food in developing countries.

1998

21

22
23
24

25

26

27
28

Acknowledgments
This work was supported by funding from Concern Worldwide. Concern
Worldwide has been engaged in the research and development of
community-based therapeutic care but has had no inuence over the text
of this review.

29

References
1
WHO. WHO child growth standards. Acta Paediatr 2006; 95 (suppl):
1101.
2
WHO. Management of severe malnutrition: a manual for
physicians and other senior health workers. Geneva: WHO, 1999.
3
UNHCR. Handbook for emergencies, 2nd edn. Geneva: UNHCR,
1999.
4
SPHERE project team. The SPHERE humanitarian charter and
minimum standards in disaster response, 2nd edn. Geneva: The
SPHERE Project, 2003.
5
Schoeld C, Ashworth A. Why have mortality rates for severe
malnutrition remained so high? BullWorld Health Organ 1996; 74:
22329.
6
Berg A. Sliding towards nutrition malpractice; time to reconsider
and redeploy. Am J Clin Nutr 1992; 57: 37.
7
UNICEF. Strategy for improved nutrition of children and women in
developing countries. New York: UNICEF, 1990.
8
Cahill GF. Starvation in man. N Engl J Med 1970; 282: 66875.
9
Forbes GB, Drenick EJ. Loss of body nitrogen on fasting.
Am J Clin Nutr 1979; 32: 157074.
10 Waterlow JC. Metabolic adaptation to low intakes of energy and
protein. Ann Rev Nutr 1986; 6: 495526.
11 Keys A. The biology of human starvation, 1st edn. Minnesota:
Minnesota Press, 1950.
12 McCance RA, Widdowson EM. Studies in undernutrition, Wuppertal
194649, 1st edn. London: Medical Research Council, 1951.
13 Winick M. Hunger disease. New York: Wiley-Interscience, 1979.
14 Waterlow JC. Protein energy malnutrition, 1st edn. London: Edward
Arnold, 1992.
15 Golden M. The eects of malnutrition in the metabolism of
children. Trans R Soc Trop Med Hyg 1988; 82: 36.
16 Golden MH, Waterlow JC, Picou D. Protein turnover, synthesis and
breakdown before and after recovery from protein-energy
malnutrition. Clin Sci Mol Med 1977; 53: 47377.
17 Reid M, Badaloo A, Forrester T, Heird WC, Jahoor F. Response of
splanchnic and whole-body leucine kinetics to treatment of children
with edematous protein-energy malnutrition accompanied by
infection. Am J Clin Nutr 2002; 76: 63340.
18 Black RE, Morris SS, Bryce J. Where and why are 10 million
children dying every year? Lancet 2003; 361: 222634.
19 Cauleld LE, de Onis M, Black RE. Undernutrition as an underlying
cause of child deaths associated with diarrhea, pneumonia, malaria,
and measles. Am J Clin Nutr 2002; 80: 19398.
20 Rice AL, Sacco L, Hyder A, Black RE. Malnutrition as an underlying
cause of childhood deaths associated with infectious diseases in
developing countries. Bull World Health Organ 2000; 78: 120721.

31

30

32

33

34

35
36
37
38

39
40
41
42

43

44

45
46
47
48
49

Pelletier DL, Frongillo EA. Changes in child survival are strongly

associated with changes in malnutrition in developing countries.
J Nutr 2003; 133: 10719.
The Bellagio Child Survival Study Group. The child survival series.
Lancet 2003; 361: 138. 2003.
UNICEF. State of the worlds children 2005. New York: UNICEF,
2005.
UNICEF. UNICEF global database on child malnutrition. http://
www.childinfo.org/areas/malnutrition/wasting.php (accessed
Dec 20, 2005).
Bhan MK, Bhandari N, Bhal R. Management of the severely
malnourished child: perspective from developing countries. BMJ
2003; 326: 14651.
International Institute of Population Sciences. National family
health survey (NFHS2),1998-99. Mumbai: International Institute of
Population Sciences, 2000.
CIA. CIA World Fact Book. http://www.cia.gov/cia/publications/
factbook/index.html (accessed Sept 10, 2006).
Manary MJ, Ndkeha MJ, Ashorn P, Maleta K, Briend A. Home
based therapy for severe malnutrition with ready-to-use food.
Arch Dis Child 2004; 89: 55761.
Pelletier DL. The relationship between child anthropometry and
mortality in developing countries: implications for policy, programs
and future research. J Nutr 1994; 124 (suppl): 2047S81S.
Chen LC, Chowdhury A, Human SL. Anthropometric assessment
of energy-protein malnutrition and subsequent risk of mortality
among preschool children. Am J Clin Nutr 1980; 33: 183645.
Cook R. Is hospital the place for the treatment of malnourished
children? J Trop Pediatr Environ Child Health 1971; 17: 1525.
Golden MHN. Severe Malnutrition. In: Weatherall DJ,
Ledington JGG, Warrell DA, eds. The Oxford textbook of medicine,
3rd edn. Oxford: Oxford University Press; 1996: 127896.
Ahmed T, Ali M, Ullah MM, et al. Mortality in severely
malnourished children with diarrhoea and use of a standardised
management protocol. Lancet 1999; 353: 191922.
Prudhon C, Briend A, Laurier D, Golden MH, Mary JY. Comparison
of weight- and height-based indices for assessing the risk of death
in severely malnourished children. Am J Epidemiol 1996; 144:
11623.
Collins S, Sadler K. The outpatient treatment of severe malnutrition
during humanitarian relief programmes. Lancet 2002; 360: 182430.
Ashworth A, Jackson A, Khanum S, Schoeld C. Ten steps to
recovery. Child Health Dialogue 1996: 1012.
WHO informal consultation. Informal consultation to review
current literature on severe malnutrition. Geneva: WHO, 2004.
WHO. Management of the child with a serious infection or severe
malnutrition : guidelines for care at the rst-referral level in
developing countries. Geneva: World Health Organization; 2000.
WHO. Improving child healthIMCI: the integrated approach.
Geneva: World Health Organization, 1997.
Chopra M, Wilkinson D. Treatment of malnutrition. Lancet 1995;
345: 788.
Wilkinson D, Scrase M, Boyd N. Reduction in in-hospital mortality
of children with malnutrition. J Trop Pediatr 1996; 42: 11415.
Khanum S, Ashworth A, Huttly SR. Controlled trial of three
approaches to the treatment of severe malnutrition. Lancet 1994;
344: 172832.
Puoane T, Sanders D, Chopra M, et al. Evaluating the clinical
management of severely malnourished childrena study of two
rural district hospitals. S Afr Med J 2001; 91: 13741.
Deen JL, Funk M, Guevara VC, et al. Implementation of WHO
guidelines on management of severe malnutrition in hospitals in
Africa. Bull World Health Organ 2003; 81: 23743.
Grellety Y. The management of severe malnutrition in Africa
(dissertation). University of Aberdeen, 2000.
Briend A. Management of severe malnutrition: ecacious or
eective? J Pediatr Gastroenterol Nutr 2001; 32: 52122.
Waterlow JC. Intensive nursing care of kwashiorkor in Malawi.
Acta Paediatr 2000; 89: 13840.
Schoeld C, Ashworth A. Severe malnutrition in children: high
case-fatality rates can be reduced. Afr Health 1997; 19: 1718.
Ashworth A, Schoeld C. Latest developments in the treatment of
severe malnutrition in children. Nutrition 1998; 14: 24445.

www.thelancet.com Vol 368 December 2, 2006

Review

50
51

52

53
54
55

56
57

58

59

60

61

62

63

64

65
66
67

68
69
70

71

72

73
74
75

Ashworth A. Treatment of severe malnutrition.

J Pediatr Gastroenterol Nutr 2001; 32: 51618.
Ashworth A, Chopra M, McCoy D, et al. WHO guidelines for
management of severe malnutrition in rural South African
hospitals: eect on case fatality and the inuence of operational
factors. Lancet 2004; 363: 111015.
Ashworth A, Sanders D, Chopra M, McCoy D, Schoeld C.
Improving quality of care for severe malnutrition. Lancet 2004; 363:
2089.
Brewster D, Manary M. Treatment of severe malnutrition. Lancet
1995; 345: 453.
WHO. WHO global health atlashuman resources for health 2005.
http://www.who.int/globalatlas/dataQuery (accessed Sept 10, 2006).
Brewster D, Manary M, Graham S. Case management of
kwashiorkor: an intervention project at seven nutrition
rehabilitation centres in Malawi. Eur J Clin Nutr 1997; 51: 13947.
World Bank. Rising to the challangesthe millenium development
goals for health. Washington: World Bank, 2004.
Kessler L, Daley H, Malenga G, Graham S. The impact of the
human immuno deciency virus type 1 on the management of
severe malnutrition in Malawi. Ann Trop Paediatr 2000; 20: 5056.
Ticklay IM, Nathoo KJ, Siziya S, Brady JP. HIV infection in
malnourished children in Harare, Zimbabwe. East Afr Med J 1997;
74: 21720.
Prazuck T, Tall F, Nacro B, t al. HIV infection and severe
malnutrition: a clinical and epidemiological study in Burkina Faso.
AIDS 1993; 7: 10308.
Mgone CS, Mhalu FS, Shao JF, et al. Prevalence of HIV-1 infection
and symptomatology of AIDS in severely malnourished children in
Dar Es Salaam, Tanzania. J Acquir Immune Dec Syndr 1991; 4:
91013.
Amadi B, Mwiya M, Musuku J, et al. Eect of nitazoxanide on
morbidity and mortality in Zambian children with
cryptosporidiosis: a randomised controlled trial. Lancet 2002; 360:
137580.
Amadi B, Kelly P, Mwiya M, et al. Intestinal and systemic infection,
HIV, and mortality in Zambian children with persistent diarrhea
and malnutrition. J Pediatr Gastroenterol Nutr 2001; 32: 55054.
Chintu C, Luo C, Bhat G, et al. Impact of the human
immunodeciency virus type-1 on common pediatric illnesses in
Zambia. J Trop Pediatr 1995; 41: 34853.
Ndekha MJ, Manary MJ, Ashorn P, Briend A. Home-based therapy
with ready-to-use therapeutic food is of benet to malnourished,
HIV-infected Malawian children. Acta Paediatr 2005; 94: 22225.
Sadre M, Donoso G. Treatment of malnutrition. Lancet 1969; 2: 112.
Lawless J, Lawless MM. Admission and mortality in a childrens
ward in an urban tropical hospital. Lancet 1966; 2: 117576.
Gueri M, Andrews N, Fox K, Jutsum P, St Hill D. A supplementary
feeding programme for the management of severe and moderate
malnutrition outside hospital. J Trop Pediatr 1985; 31: 10108.
Brewster D. Improving quality of care for severe malnutrition.
Lancet 2004; 363: 208889.
Cook R. The nancial cost of malnutrition in the Commonwealth
Caribbean. J Trop Pediatr 1968; 14: 6065.
Roosmalen-Wiebenga MW, Kusin JA, de With C. Nutrition
rehabilitation in hospitala waste of time and money? Evaluation
of nutrition rehabilitation in a rural district hospital in southwest
Tanzania: I, short-term results. J Trop Pediatr 1986; 32: 24043.
Roosmalen-Wiebenga MW, Kusin JA, de With C. Nutrition
rehabilitation in hospitala waste of time and money? Evaluation
of nutrition rehabilitation in a rural district hospital in South-west
Tanzania: II, long-term results. J Trop Pediatr 1987; 33: 2428.
Reneman L, Derwig J. Long-term prospects of malnourished
children after rehabilitation at the Nutrition Rehabilitation Centre of
St Marys Hospital, Mumias, Kenya. J Trop Pediatr 1997; 43: 29396.
Collins S. Changing the way we address severe malnutrition during
famine. Lancet 2001; 358: 498501.
Bengoa JM. Nutrition rehabilitation centres. J Trop Pediatr 1967; 13:
16976.
King KW, Fougere W, Webb RE, Berggren G, Berggren WL,
Hilaire A. Preventive and therapeutic benets in relation to cost:
performance over 10 years of Mothercraft Centers in Haiti.
Am J Clin Nutr 1978; 31: 67990.

www.thelancet.com Vol 368 December 2, 2006

76

77

78

79

80

81

82

83

84

85

86

87

88
89
90
91

92

93

94

95
96

97

98

Beghin ID, Viteri FE. Nutritional rehabilitation centres: an

evaluation of their performance. J Trop Pediatr Environ Child Health
1973; 19: 40316.
Beaudry-Darisme M, Latham MC. Nutrition rehabilitation
centersan evaluation of their performance.
J Trop Pediatr Environ Child Health 1973; 19: 299332.
Pecoul B, Soutif C, Hounkpevi M, Ducos M. Ecacy of a therapeutic
feeding centre evaluated during hospitalization and a follow-up
period, Tahoua, Niger, 19871988. Ann Trop Paediatr 1992; 12: 4754.
Heikens GT, Schoeld WN, Dawson S, Grantham-McGregor S. The
Kingston project: Igrowth of malnourished children during
rehabilitation in the community, given a high energy supplement.
Eur J Clin Nutr 1989; 43: 14560.
Heikens GT, Schoeld WN, Dawson SM, Waterlow JC. Long-stay
versus short-stay hospital treatment of children suering from
severe protein-energy malnutrition. Eur J Clin Nutr 1994; 48: 87382.
Ashworth, A. Community-based rehabilitation of severely
malnourished children: a review of successful programmes.
London: London School of Hygiene and Tropical Medicine, 2001.
Ashworth, A. Ecacy and eectiveness of community-based
treatment of severe malnutrition. Food Nutr Bull 2006; 27 (suppl):
S2448.
Ahmed, T. Community-based nutritional rehabilitation without
food distribution: experience from Bangladesh, in WHO, UNICEF
and SCN informal consultation on community-based management
of severe malnutrition in children. http://www.who.int/
child-adolescent-health/ (accessed Sept 10, 2006).
Ashworth A, Khanum S. Cost-eective treatment for severely
malnourished children: what is the best approach?
Health Policy Plan 1997; 12: 11521.
Bredow MT, Jackson AA. Community based, eective, low cost
approach to the treatment of severe malnutrition in rural Jamaica.
Arch Dis Child 1994; 71: 297303.
Briend A, Lacsala R, Prudhon C, Mounier B, Grellety Y,
Golden MHN. Ready-to-use therapeutic food for treatment of
marasmus. Lancet 1999; 353: 176768.
Briend A. Highly nutrient-dense spreads: a new approach to
delivering multiple micronutrients to high-risk groups. Br J Nutr
2001; 85 (suppl 2): S17579.
Briend A. Treatment of severe malnutrition with a therapeutic
spread. Field Exchange 1997; 2: 15.
Collins S, Henry CJK. Alternative RUTF formulations. Emergency
Nutrition Network 2004; special supplement 2: 3537.
Fellows P. Local production of RUTF. Emergency Nutrition
Network 2004; special supplement 2: 3335.
Sandige H, Ndekha MJ, Briend A, Ashorn P, Manary MJ.
Home-based treatment of malnourished Malawian children with
locally produced or imported ready-to-use food.
J Pediatr Gastroenterol Nutr 2004; 39: 14146.
Diop EHI, Dossou NI, Ndour MM, Briend A, Wade S. Comparison
of the ecacy of a solid ready to use food and a liquid milk-based
diet for the rehabilitation of severely malnourished children: a
randomized trial. Am J Clin Nutr 2003; 78: 30207.
Ciliberto MA, Sandige H, Ndekha MJ, et al. Comparison of
home-based therapy with ready-to-use therapeutic food with
standard therapy in the treatment of malnourished Malawian
children: a controlled, clinical eectiveness trial.
Am J Clin Nutr 2005; 81: 86470.
Collins S. Community-based therapeutic carea new paradigm for
selective feeding in nutritional crises: Humanitarian Policy Network
paper 48. London: Overseas Development Institute, 2004.
Khara T, Collins S. Community-therapeutic care (CTC). Emergency
Nutrition Network 2004; special supplement 2: 155.
Emergency Nutrition Network. ENN report on an inter-agency
workshop. http://www.ennonline.net/docs/CTCreport.pdf (accessed
Sept 10, 2006).
Grobler-Tanner C, Collins S. Community therapeutic care (CTC): a
new approach to managing acute malnutrition in emergencies and
beyond. Washington DC: Food and Nutrition Technical Assistance
Project, Academy for Educational Development, 2004.
Guerrero S, Mollison S. Engaging communities in emergency
response: the CTC experience in Western Darfur. In Humanitarian
Exchange. Humanitarian Policy Network eds. London: Overseas
Development Institute, 2005: 2022.

1999

Review

99

100
101

102

103

104

105

106

2000

Briend A, Dykewicz C, Graven K, Mazumder RN, Wojtyniak B,

Bennish M. Usefulness of nutritional indices and classication in
predicting death of malnourished children. BMJ 1986; 293: 37376.
Alam N, Wojtyniak B, Rahaman MM. Anthropometric indicator and
risk of death. Am J Clin Nutr 1989; 49: 88488.
Briend A, Garenne M, Maire B, Fontaine O, Dieng K. Nutritional
status, age and survival: the muscle mass hypothesis.
Eur J Clin Nutr 1989; 43: 71526.
Vella V, Tomkins A, Ndiku J, Marshal T, Cortinovis I.
Anthropometry as a predictor for mortality among Ugandan
children, allowing for socio-economic variables. Eur J Clin Nutr
1994; 48: 18997.
WHO. Report of an informal consultation on the community-based
management of severe malnutrition in children. http://www.who.
int/child-adolescent-health/publications/NUTRITION/CBSM.htm.
(accessed Sept 10, 2006).
Myatt M, Khara T, Collins S. A review of methods to detect cases of
severely malnourished children in the community for their
admission into community-based therapeutic care programs.
Food Nutr Bull 2006; 27 (suppl): S723.
Velzeboer MI, Selwyn BJ, Sargent S, Pollitt E, Delgado H. The use
of arm circumference in simplied screening for acute
malnutrition by minimally trained health workers. J Trop Pediatr
1983; 29: 15966.
Berkley J, Mwangi I, Griths K, et al. Assessment of severe
malnutrition among hospitalized children in rural Kenya:
comparison of weight for height and mid upper arm circumference.
JAMA 2005; 294: 59197.

107 Pelletier DL, Frongillo EA Jr, Schroeder DG, Habicht JP. The eects
of malnutrition on child mortality in developing countries.
Bull World Health Organ 1995; 73: 44348.
108 Bairagi R. On validity of some anthropometric indicators as
predictors of mortality. Am J Clin Nutr 1981; 34: 259294.
109 Collins S, Yates R. The need to update the classication of acute
malnutrition. Lancet 2003; 362: 249.
110 Myatt M, Feleke T, Sadler K, Collins S. A eld trial of a survey
method for estimating the coverage of selective feeding programs.
Bull World Health Organ 2005; 83: 2026.
111 Van Damme W. Medical assistance to self-settled refugees. Guinea
19901996. Antwerp: ITG Press, 1998.
112 Jha P, Bangoura O, Ranson K. The cost-eectiveness of forty health
interventions in Guinea. Health Policy Plan 1998; 13: 24962.
113 Tectonidis M. Crisis in Nigeroutpatient care for severe acute
malnutrition. N Engl J Med 2006; 354: 22427.
114 Guerrero S, Bahwere P, Sadler K, Collins S. Integrating CTC and
HIV/AIDS Support in Malawi. Field Exchange 2005; 25: 810.
115 Collins S, Sadler K, Dent N, et al. Key issues in the success of
community-based management of severe malnutrition.
Food Nutr Bull 2006; 27: S4982.
116 World Bank. World development report 1993, investing in health.
Oxford: Oxford University Press, 1993.
117 Hamer C, Kvatum K, Jeries D, Allen S. Detection of severe
protein-energy malnutrition by nurses in The Gambia.
Arch Dis Child 2004; 89: 18184.

www.thelancet.com Vol 368 December 2, 2006